Electricity generation from moss with light-driven
microbial fuel cells
Pablo Ampudia Castresanaa,b, Sara Monasterio Martineza,b, Emma Freemanb, Salvador
Eslavab, Mirella Di Lorenzoa,b*
aCentre for Biosensors, Bioelectronics and Biodevices, University of Bath, Bath, BA2
7AY, UKbDepartment of Chemical Engineering, University of Bath, Bath, BA2 7AY, UK
* Corresponding author.
E-mail address: [email protected] (M. Di Lorenzo)
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Abstract
Fossil fuel depletion, increasing energy demands and concerns on greenhouse gas
emissions heavily stress the search for sustainable and green energy alternatives. Plant
microbial fuel cells (PMFCs) are an attractive carbon-neutral energy conversion
technology that can generate useful electricity from microorganisms naturally present in
soil and from the organic matter produced by plants during photosynthesis. We report
an innovative membrane-less light-driven PMFC and demonstrate its ability to harvest
energy from moss. The PMFC implements a CuO-Cu2O photocatalyst at the cathode,
leading to a peak power output approximately 14 times higher than the case of no
photocatalyst and a reduction in the Ohmic losses of approximately 50%. A light/dark
cycle trend is observed, which help distinguish between the anodic and the
photocatalytic contribution to the overall current generated. The use of a protective
layer to prevent the photocatalyst leaching is also tested. The simplicity and cost-
effectiveness of the design proposed overcomes the cost limitations of other PMFCs
previously reported, thus facilitating their future scale up.
Graphical Abstract
x
x
Keywords: Plant microbial fuel cell, Bioenergy, Photocatalyst, Copper oxide, Nafion.
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1 INTRODUCTION
Increasing energy demands, along with concerns about greenhouse gas emissions
and fossil fuels depletion, have led to strict renewable energy policy targets worldwide.
In Europe, for example, the Renewable Energy Directive has set a goal of 20% energy
generation from renewable sources by 2020. These targets force the interest into the
development of innovative energy technologies that can help guarantee their
achievement. In this context, plant microbial fuel cells (PMFCs) have great potential as
a carbon-neutral bioenergy conversion technology. Nevertheless, the technology is still
at a very early stage of development and its potential needs to be explored.
PMFCs convert the chemical energy stored in organic matter naturally present in
soil directly into electrical energy, thanks to the action of electrochemically active
bacteria (EAB) [1,2]. In particular, EAB at the anode oxidase the organic matter
supplied by plants during photosynthesis, thus exchanging electrons (eb-) and
transferring protons (H+) [1,3]. The eb- travel across an external circuit to the cathode,
generating electricity, while H+ diffuse to the cathode through the soil. At the cathode,
oxygen reacts with the eb- and H+ to produce H2O. The recent progress on PMFCs with a
carbon-based cathode is summarised in Table S1 in Supplementary Information (SI).
Successful pilot experiments in natural environments, such as green roofs [4], floating
bodies of water [5] and wetlands [6], have been reported. Despite attractive features,
such as cost-effectiveness, sustainability and limited or null environmental footprint, the
PMFCs reported so far are, however, still limited by poor power outputs [1].
The system performance is influenced by the configuration used, the utilisation of
cation-exchange-membranes, the electrode materials, as well as the properties of the soil
in which the PMFC is installed. The use of an Oxygen Reduction Reaction (ORR)
catalyst at the cathode is also important and can improve the overall performance of the
PMFC system. Several ORR catalysts have been tested in MFCs [7]. Bare carbon
materials, such as for example carbon nanotubes [8,9], tend to favour a slow 2e- ORR
pathway, whereas both 2e- and 4e- ORR pathways can occur simultaneously or
individually on carbon activated with metal-free catalysts, such as S-doped graphene
[10] and nitrogen [11], and metals, such as Pt [12,13] and Co [14]. The 2e- pathway is
unfavourable from an energy generation point of view, due to the higher overpotential
and smaller Faradaic efficiency that it implies. Consequently, the most typical ORR
catalyst used in fuel cells is platinum (Pt), which accounts for the largest cost associated
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with the technology [15,16]. Extensive research has, therefore, been conducted in the
search for Pt-free, low-cost and efficient ORR catalyst alternatives [17].
In this work, we present an innovative membrane-less and light-driven PMFC with
a photoactive cathode in direct contact with soil. A mix of copper oxides (CuO and
Cu2O) has been used as the photocatalyst, due to its suitable bandgaps (Eg = 1.2 and 2.1
eV, resp.) and its band-edge positions with respect to the redox potential of the anodic
biofilm [15]. The integration of a p-type semiconductor material at the cathode of the
PMFC leads to the generation of electron-hole pairs (e-/h+) under irradiation. These
holes remain in the valence band (VB) of the semiconductor, while electrons (e -)
injected into the conduction band (CB) can either reduce electron acceptors at the
semiconductor/electrolyte interface, or recombine with h+ accumulated in the VB [18–
20]. During irradiation, the transfer of eb- generated at the anode is enhanced by the h+ at
the VB of the p-type semiconductor. In this study, Pleurocapous moss was chosen as
the model plant, because it grows relatively fast, tend to form spreading carpets rather
than erect tufts and tough does not require particular conditions of humidity,
temperature and soil nutrients. The electrochemical performance of the light-driven
PMFCs are investigated with and without photocatalyst at the cathode. The effect of
protecting the copper oxide photocatalyst with the ionic polymer Nafion is also
investigated.
2 EXPERIMENTAL
2.1 Materials
All reagents used were of analytical grade and purchased from Sigma Aldrich, Alfa
Aesar and VWR Chemicals.
Pleurocapous moss was chosen as the organic matter supplier for the PMFCs,
because it is widely found in wetlands, urban and rural environments. Both moss and
soil were collected from the University of Bath campus (Bath, UK). The soil used was
characterised by a low-trace concentration of nitrate (NO3−) and phosphate (PO43−¿¿) ions,
high concentration of potassium (K+) ions and a pH value between 5 and 6, as indicated
by colorimetric and turbidimetric methods (NPK Soil Test Kit-HI3895-Hanna
Instruments). The soil conductivity, κ, determined with the Thermo Scientific-Orion
conductivity probe, is 387.8 ± 3.96 µScm-1. The percentage of water content in soil
(WCsoil =22.9% ± 8.17) was estimated from the difference in weight of the soil sample
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before (mwet soil) and after incubation at 105 °C for 12 h (mdry soil), according to Equation 1
[21]:
WCsoil(%)=( mwet soil−mdry soil/mdry soil )100 (1)
2.2 PMFC design and fabrication
The soil and the moss were placed in PVC containers (6 cm width x 9 cm length x 3
cm height). Each container hosted a PMFC, which consisted of an anode and a cathode
electrode at a parallel distance of 0.5 cm from each other. The anode was immersed in
the soil, while the cathode was exposed to air (Figure 1).
The anode consisted of a 2 x 2 cm rectangular piece of carbon felt (CF, 7 mm
thickness, Online Furnace Services Ltd). Prior to be used, CF was pre-treated to
enhance the hydrophilicity and roughness of the carbon nanofibres, as previously
described [22]. Both the hydrophilicity and roughness would enhance the biofilm
attachment onto the electrode fibres and mass transport phenomena within the electrode
structure, leading to a better bacterial cells distribution throughout the 3D electrode and,
consequently, better electrochemical performance. With this purpose, CF was first
soaked in pure ethanol for two days, and subsequently in an aqueous solution of
ammonium peroxydisulfate (0.87 M) and sulfuric acid (1.88 M) for 15 minutes.
Afterwards, CF was thoroughly washed with Milli-Q water and finally thermally treated
in a muffle furnace at 450 C for 30 min in air atmosphere. The so-treated CF was
stored in Milli-Q water at room temperature until used.
Different materials were employed as the cathode, leading to four different types of
PMFC (Figure 1A) : PMFC-1, with a cathode made of CF (2 x 2 x 0.70 cm); PMFC-2,
with a cathode made of bare fluorine-doped tin oxide coated glass (glass/FTO, 3 x 1 cm,
Sigma-Aldrich); PMFC-3, with a glass/FTO cathode treated with copper oxide; and
PMFC-4, with a glass/FTO cathode treated with copper oxide and Nafion (Nf). These
cathodes were named FTO, FTO/CuxO and FTO/CuxO/Nf. The copper oxide
photocatalyst layer is indicated as CuxO, since it is composed of a CuO-Cu2O mixture
(Figure 2).
The glass/FTO slides were sonicated 30 min in acetone, washed in Milli-Q water
and heated at 500 °C for 1 h. To functionalise FTO with a film of Cu xO photocatalyst, a
suspension containing 0.3 g CuO (nanopowder, particle size < 50 nm, Sigma Aldrich), 4
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mL ethanol, 5.3 mL Triton 100-X and 10.6 mL tetrahydrofuran was prepared and
sonicated overnight prior to use. 100 μL (0.002 g of CuO) of this solution was drop-
casted onto 2 cm2 glass/FTO, allowed to dry in air at room temperature and then heated
to 500 °C for 1 h in air. For the PMFC-4 configuration, the FTO/CuxO surface was
coated with Nafion® perfluorinated resin solution (5 wt. % in lower aliphatic alcohols
and 45% in water, Sigma Aldrich), drop-casting (100 µL, 0.005 g of Nafion) onto the
electrode surface and allowing it to dry in air at room temperature overnight. The
functionalized area of the glass/FTO slides was 2 cm2. The remaining area (1 cm2) was
used for the electrical contact.
Figure 1. Schematic of the PMFC and disposition of materials (CF, FTO, CuxO and Nf) at the cathode (A). (B) Photograph of the PMFC-4 tested in this study, showing the: PVC container; PMFC (1); moss (2); red anode and cathode (black and red) banana connectors (3); external resistance (4).
2.3 PMFC operation
To polarise the cell, the anode and cathode were connected to an external circuit,
characterised by an external resistance of 510 . The cell voltage over time was
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monitored with a data acquisition system (ADC-24 Pico data logger, Pico technology,
UK). Titanium wire (0.25 mm dia., Alfa Aesar) was used for the electrical contacts, and
a non-conductive epoxy resin (Evo-Stik) was used to isolate the electrical contact and to
avoid any interference with the electrolyte.
To simulate light/dark cycles, the PMFCs were illuminated with an LED lamp
(Tingkam A4 ultra-thin box, rate power density: 4.7 mW cm-2), placed at a distance of
10 cm from the cathode, with an illumination period of 12 h per day. An ILT1400 meter
with a SEL623/QNDS1/W broadband detector was used to measure the light intensity
towards the surface of the cathode, which resulted to be 0.67 mW cm-2. The PMFCs
were operated at room temperature, which ranged within 17 - 20 °C.
The photocurrent produced by the cell (Icell) was calculated as follows:
I cell=I cellday−I cell
night (2)
Where I cellday was the current observed under irradiation and I cell
night was the current
generated in the dark.
2.4 Electrochemical analyses and electrodes characterisation
The photoactivity of the CuxO photocathodes was tested by linear sweep
voltammetry (LSV) in a 0.1 M Na2SO4 aqueous solution (pH=6.6) with a potentiostat
(CompactStat, Ivium Technologies). A three-electrode set-up was used, with the CuxO
electrode as the working electrode and Pt wire and Ag/AgCl as counter and reference
electrodes, respectively. The LSV was run from 0 to -0.6 VAg/AgCl, under chopped solar
illumination (100 mWcm-2), obtained with an AM1.5 filtered 300W Xenon lamp source.
LSV tests were also performed in soil to assess the photoactivity of the cathodes in
a simulated real-environment. In this case, a stainless-steel gauze (4 x 4 cm, 20 mesh
woven from 0.382 mm dia. wire, Alfa Aesar) and a Pt wire (1.5 mm dia.) were used as
counter and pseudo-reference electrodes, respectively, while the CuxO electrode was the
working electrode. A Pt pseudo-reference electrode was used for the electrochemical
characterization, in situ (i.e. in the soil). Contrarily to conventional reference electrodes
(silver/silver chloride, copper/copper sulfate or calomel electrode), which require
immersion in an electrolyte contained by a liquid junction [22, 23], Pt can be used in
non-liquid electrolytes, with high ohmic resistance. Conventional reference electrodes
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cannot be used with solid-state electrochemical cells (i.e. cells in soil pastes). On the
other hand, there is no liquid junction potential associated to the Pt pseudo-reference
electrode, and usually there is no contamination of the soil by solvent molecules or ions
that conventional reference electrodes might transfer.
The photocurrent density (i) was calculated with respect to the nominal geometric
area of the cathode (13.6 cm2 for CF; 2 cm2 for FTO, FTO/CuxO and FTO/CuxO/Nf).
The performance of the anodic biofilm was investigated in soil by cyclic
voltammetry (CV) measurements using PGSTAT 302 (Metrohm-Autolab, The
Netherlands), at a scan rate of 2 mVs-1, right after the cell set-up (day 1) and after six
days of operation (day 6). The tests were performed by setting the anode as the working
electrode, while using stainless-steel grid (4 x 4 cm) as counter electrode and a Pt wire
(1.5 mm dia.) as pseudo-reference.
Polarisation tests were performed by applying different external loads to the fuel
cells (from 900 to 15 k) with a resistor box (Cropico RM6 Decade Box, RS
Components), and measuring the corresponding cell voltages. Prior to this test, the
PMFCs were left under open circuit for no more than 2 h until a steady-state voltage
was observed. Measurements were conducted under dark or irradiation (with a LED
lamp) conditions, to evaluate the influence of the photocatalyst at the cathode on the
overall performance of the PMFCs. Ohm’s law (I = V/R) was used to calculate the
current, I, (where V and R indicate the cell voltage and resistance, respectively). For
easier comparison, the power density of each PMFC was normalised by the respective
cathode nominal geometric area.
Electrochemical Impedance Spectroscopy (EIS) measurements were performed in
the soil at the open circuit potential under dark and irradiation conditions. The
frequency of the AC signal was varied from 50 x103 to 0.1 Hz with an amplitude of 10
mV. In these tests, the cathode was used as the working electrode and the anode as
counter electrode.
The morphology of both the electrodes and the biofilm (after operation) was
visualised by Scanning Electron Microscopy, SEM (Jeol JSM-6480LV). The biofilm
was fixed by following a procedure previously described [23]. All samples were coated
with gold prior to imaging.
X-ray diffraction (XRD) patterns of the glass/FTO and CuxO film were obtained
from a BRUKER AXS D Advance diffractometer using a Vantec-1 detector and CuKα
radiation with a range of 2θ from 20° to 80°.
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3 RESULTS AND DISCUSSION
3.1 Performance of the CuxO-functionalised electrodes
The use of a photocatalyst at the cathode of a plant microbial fuel cell was
investigated to improve the electrochemical performance. Four different types of
PMFCs were tested with differences in the cathode electrode used: CF (PMFC-1), FTO
(PMFC-2), FTO/CuxO (PMFC-3) and FTO/CuxO/Nf (PMFC-4). PMFC-1 and PMFC-2
were tested as control. In PMFC-4, a layer of Nafion was used to prevent the diffusion
of redox-active interferences to the cathode and as a protective coating to prevent CuxO
leaching into the soil [24].
The morphology of the CuxO-based photocathodes is shown in Figure 2. The
FTO/CuxO electrode is characterised by a granulated structure, with particles size below
the micron range. The granulated structure is softened with the coverage of Nafion in
FTO/CuxO/Nf electrodes. The XRD pattern of the copper oxide film on glass/FTO, after
the thermal treatment at 500 °C, is given in Figure 2C. A film consisting of a mixture of
CuO and Cu2O was obtained after depositing the CuO suspension and annealing the
films. The film pattern of the FTO/CuxO electrode clearly shows peaks at 2ɵ= 35.9,
2ɵ=36.8 and 2ɵ=39.1, which correspond to (110) CuO, (111) Cu2O and (111) CuO
crystal planes, respectively [25].
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A B
1 m1 m
**
20 30 40 50 60 70 80
Inte
nsity
(a.u
)
2ɵ ( degree)
CuOFTO
FTO/CuO
FTO
˟
˟*
110
002
111
˟
˟ ˟˟ ˟
˟˟ ˟ ˟ ˟
˟ *
Cx
Figure 2. SEM images of the FTO/CuxO (A) and (B) FTO/CuxO/Nf electrodes (SEM magnification x10000). (C) X-Ray Diffraction (XRD) pattern of blank FTO and FTO/CuxO electrodes after the thermal treatment (500 °C for 1 h in air).
Both the FTO/CuxO and FTO/CuxO/Nf electrodes were electrochemically
characterised by LSV, under chopped irradiation in an aqueous solution containing
0.1M Na2SO4 (Figure 3A). The observed increase in the reduction current under
irradiation confirms the photoactivity of CuxO [26]. Nonetheless, the FTO/CuxO/Nf
electrode shows photocurrents over two times higher than the FTO/CuxO electrode, thus
suggesting that Nafion improves the reduction reaction that take place at the CuxO
surface by facilitating the transport of protons [27–29] towards the CuxO active sites.
The performance of the FTO/CuxO/Nf electrode was also tested in soil (Figure 3B).
In this case, a decrease in the current density was observed. This result can be attributed
to the fact that the soil has a conductivity, κsoil, of 387.8 µS cm-1, much lower than the
used 0.1 M Na2SO4 aqueous solution (15.5 103 µS cm-1). Charge transfer resistance
(RCT) at the soil/anode interface is also expected to be higher, since RCT increases in
electrolytes with poor water content [30].
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-5
-4
-3
-2
-1
0
1-0.6 -0.5 -0.4 -0.3 -0.2 -0.1 0
i ( m
A cm
-2)
Potential ( V ) vs. Ag/AgCl
FTO/CuO
FTO/CuO/Nf
-5
-4
-3
-2
-1
0
1-0.6 -0.5 -0.4 -0.3 -0.2 -0.1 0
i ( m
A cm
-2)
Potential ( V ) vs. pseudoreference Pt electrode
FTO/CuO/Nf
A B
x
x x
Figure 3. LSV tests in: (A) 0.1M Na2SO4 (pH=6.6) (FTO/CuxO and FTO/CuxO/Nf); (B) soil (FTO/CuxO/Nf). Light on/off periods are indicated by light/grey shaded regions. Scan rate 20 mVs-1.
3.2 PMFCs operation
Figure 4A shows the output current generated by the four PMFCs over a period of
six days. Generally, after five days of operation, a pseudo-steady state current was
observed, thus suggesting the build-up of an electroactive biofilm onto the anode
surface [23]. All the cells follow a light/dark cycle, with greater current values under
irradiation conditions. The current difference under light with respect to the dark is,
however, much more marked in PMFC-3 and PMFC-4, because of the photoactivity of
CuxO. This difference reaches a maximum value of 1.39 ± 0.40 µA and 0.61 ± 0.33 µA
for PMFC-3 and PMFC-4, respectively, while the light/dark current difference for
PMFC-1 and PMFC-2 are only 0.21 µA ± 0.08 µA and 0.04 ± 0.05 µA, respectively.
Figure 4B reports the current peaks generated during the light/dark cycles by PMFC-3
and PMFC-4, while the comparison of these values with the controls (PMFC-1 and
PMFC-2) is given in Figure S1 in the Supplementary Information.
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0
1
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0 1 2 3 4 5 6
Cell
Cur
rent
( µ
A )
Time ( days)
PMFC- 4PMFC- 3PMFC- 2PMFC- 1
A
0
1
2
3
4
5
6
7
1 2 3 4 5 6
Cell
Cur
rent
( µ
A )
Time (days)
PMFC-3PMFC-4 B
Figure 4. (A) Current generated by the PMFCs during six days of operation under light/dark cycles; Light on/off periods are indicated by light/grey shaded regions; Rext =510 Ω. Data is the average of two replicates, with a maximum standard error on the averaged cell current of: 0.24 for PMFC-1; 0.84 for PMFC-2; 0.45 for PMFC-3 and 0.80 for PMFC-4. (B) Current peaks generated during the dark (pattern fill) and light (solid fill) cycles by PMFC-3 and PMFC-4 over a period of six days of operation. Error bars refer to standard error between two replicates.
The electroactive activity of the anodic biofilm was confirmed by in-situ CV tests,
performed on day zero and day six of operation [31]. A significant improvement in the
electrochemical activity was observed with the biofilm growth [32]. The CV after six
days of acclimatisation shows current peaks at 0.2 and 0.7 V vs pseudo-reference Pt
electrode, which are not observed on day one (Figure 5). Moreover, SEM images of the
anodes after six days of operation, show a biofilm attached onto the carbon fibres (Figure 6).
Figure 5. CV performed at a CF anode of two cells (PMFC-3 and PMFC-4) in the soil, on day 0 (dotted line) and day 6 (solid line) of operation; four cycles were performed at a scan rate: 2 mVs -1. Error bars refer to two replicates.
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100 m 100 m
BA
Figure 6. SEM images of the CF electrode before (A) and after (B) six days of operation. (SEM magnifications: x200; x10000 for the inserts)
Three main processes account on the performance of the PMFCs and should be
used to explain the difference in the current generated by each design tested: the
generation and transfer of bio-electrons (eb-) at the anode; the photo-generation of
electron/hole (e-/h+) pairs at the photocathode; and the generation of organic matter (the
fuel for the anodic biofilm) during the photosynthesis. Figure 7 shows a schematic of
the proposed working mechanism in the different PMFCs.
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Figure 7. Schematic of the proposed charge transfer mechanism in the PMFCs when no photocatalyst at the cathode is used (A and B) and when a photocatalyst is used (C and D), under irradiation (A and C) and dark (B and D) conditions.
For each PMFC, the efficiency of the anodic process is related to the capability of
the EAB to oxidise organic matter (CxHyOz) and generate bio-electrons, eb-, and protons,
H+. The eb- flow towards the cathode through the external circuit, while H+ diffuse to the
cathode surface through the soil. During the photosynthesis, moss roots excrete organic
matter, CxHyOz roots, used as a fuel by the EAB [33], and oxidised to generate eb- (Figure
7B and 7D). In the absence of light, both non-photoactive (CF and FTO) and
photoactive (FTO/CuxO and FTO/CuxO/Nf) cathodes act as eb- conductor materials
(Figure 7A and 7C). On the other hand, the photocathode surface is activated under
irradiation and e-/h+ separation is achieved, leading to a higher cathode potential with
respect to the bio-anode [34]. In the acidic conditions of the soil (pH=5-6), the
photoinduced e- from the conduction band (CB, -4.2 eV and -3.3 eV, for CuO and Cu2O
respectively) of CuxO reduce dissolved oxygen (ORR potential: -4.6 eV) into OH- or
water at the cathode/soil interface [17,35], while h+ at the valence band (VB, -5.45 eV
and -5.4 eV for CuO and Cu2O respectively) recombine with the eb- (Figure 7D),
avoiding their recombination with photoinduced e- [36]. In this process, the enhanced
transfer of eb- to the cathode during day time is ascribed to the presence of photo-
generated h+ [15].
The current increase with time shown in Figure 4A suggests that the break-down of
the organic matter by the EAB at the anode may be the main process involved in the
bio-electricity generation in the absence and presence of light. Under irradiation,
however, the release of CxHyOz roots further increases the contribution of the anodic
reaction to the current generation. Consequently in the case of PMFC-1 and PMFC-2,
the fluctuations in the output current during the light/dark cycles depend on the
variation on fuel availability generated by photosynthesis (Figure 7A and 7B). Since
temperature was relatively stable throughout the experiments, the results highlight the
benefit of using plants as organic matter supply in biological fuel cells [37].
In PMFC-3 and PMFC-4, instead, a more pronounced current increase is observed
during the light cycles, due to the generation of e-/h+ pairs in the CuxO. In these PMFCs,
therefore, the photocatalyst allows an increase on the reductive activity of eb-, which
would favour the cathodic reduction reactions [36].
Overall, the highest current output was generated by PMFC-4 (Figure 4B), which
differs from PMFC-3 only in the presence of a Nafion layer covering the CuxO at the
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cathode. Nafion is an ionomer that has been widely explored as a H+ conductor in fuel
cells, due to its high ionic conductivity and chemo-thermo-mechanical stability [38,39].
Nafion have been consequently widely implemented in microbial fuel cells as proton
exchange membranes [40].
In PMFC-4, Nafion might also act as a protective layer and prevent CuxO leaching,
which can be harmful to the microorganisms and, consequently, can affect the
generation of eb- (anodic reaction) [41,42]. By enhancing proton diffusion to the CuxO
surface, the Nafion layer favours the reaction between electron acceptor species, H+ and
e- at the CuxO/electrolyte interface, which accelerates the consumption of photo-
generated carriers. The photo-generated holes in the VB of the CuxO can, therefore, also
recombine with bio-electrons generated at the anode (Figure 7D), thus simultaneously
increasing the e-/h+ recombination resistance within the CuxO layer [15].
When comparing the performance of PMFC-3 with PMFC-4, the average
photocurrent (current difference between light and dark conditions) generated by
PMFC-3 (the one without Nafion) during six days of operation was found to be higher
(IPMFC-3 : 1.43 ± 0.23 and IPMFC-4 : 0.63 ± 0.24). A possible reason for this trend might be
CuxO leaching from the cathode, which might inhibits bacteria metabolism and
consequently the anodic contribution to the current production. This would then result
in a decrease in the current output in the dark and, therefore, in an increase in the
photocurrent produced under irradiation.
Polarisation tests were performed for the PMFCs (Figure 8A and 8B) after six days
of operation. Since PMFC-1 and PMFC-2 have no photocatalyst at the cathode, no light
is required to activate them. As such, the polarisation tests were performed in the dark
for PMFC-1 and PMFC-2, and under the light for PMFC-3 and PMFC-4. As shown in
Figure 8A, the maximum power and current densities generated by PMFC-1 and -2 in
the dark are 10 times lower that the values obtained by PMFC-3 and -4. These values
are one order of magnitude higher than those observed with other MFCs using FTO
cathodes or a Pt-functionalised carbon cathode [15].
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Figure 8. Power (A) and (B) polarisation curves under dark (PMFC-1 and PMFC-2) and irradiation (PMFC-3 and PMFC-4) conditions. Power and current densities refer to the geometric cathodic electrode area. Error bars refer to the standard error from two replicates. (C) Electrochemical impedance spectroscopy tests of PMFC-3 and PMFC-4 under irradiation (LED lamp) and equivalent circuit diagram. Inset: magnification at high frequencies.
The largest power density was obtained with PMFC-4 (2.5 mW m-2). This is a much
higher power than the one obtained with a dual chamber MFC with a CuInS2
photocathode (0.108 mW m-2, [15]), and is comparable to the power obtained with a
dual chamber MFC with a TiO2 photocatalyst as cathode (6 mW m-2, [34]). TiO2 suffers,
however, from lower quantum efficiency and photoactivity performance under solar
irradiation, due to its narrow bandgap (Eg = 3.0-3.2 eV) [15,43]. The CuO-Cu2O
photocatalyst (Eg = 1.2 and 2.1 eV, resp.) allows more efficient visible light absorption
and therefore is more suitable for light-driven PMFC systems.
The open circuit voltages obtained with PMFC-3 and PMFC-4 are also higher than
the controls (Figure 8B). The polarisation tests reveal a great dependence of the
electrochemical performance of the PMFCs on the cathode activity. For all the PMFCs,
ohmic resistances (RΩ) dominate the process, mainly due to the low conductivity of the
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soil and to the electrical resistance of the electrodes [44]. Nonetheless, much larger
ohmic losses are observed when CF and FTO are used as cathodes.
The internal resistance of the systems (Rint= -∆E/∆I), which comprises both ohmic
(RΩ) and polarization resistances (Rp) [45], was estimated from the slope of the ohmic
region in the polarisation curves in Figure 8B [46]. An almost linear trend characterized
the polarization curves for all the PMFCs (Figure 8B), which suggests that RΩ
dominates the process [46]. This might be a result of the low conductivity of the soil
and of the electrical resistance of the electrodes [45]. Much larger Rint are observed
when CF and FTO are used as cathodes. The use of CuxO at the cathode (PMFC-3)
reduced Rint from 94.5 kΩ (value for FTO cathode, PMFC-2) to 64 kΩ (under
irradiation conditions). This value was further reduced to 47.5 kΩ when a layer of
Nafion was used (PMFC-4). This result suggests that the output power generated by the
PMFCs is limited not only by ohmic resistance related to the ion transportation through
the soil (RΩ), but also by the resistance to charge transfer at the cathode/electrolyte
interface (Rp).
If compared with other soil/plant microbial fuel cells, the power generated by our
system seems low (Table 1S). A direct comparison is, however, difficult due to
differences in configuration and materials used. The PMFC presented in this work is,
however, characterised by an extremely simple and cost-effective design, as no
membrane and/or expensive ORR catalyst are used. The Ohmic losses at the cathode,
which can be caused by ionic resistance in the catholyte (soil) [43], are predominant in
our system. The mass transfer (i.e., transport of O2 or reaction products) in the
cathode/anode vicinity can be also a limiting factor. A direct comparison with those
PMFCs is, however, difficult, due to several differences in working conditions and fuel
cell designs. Moreover, the higher power densities previously reported can also be a
consequence of longer operation times (e.g. 120 days [45], compared to the six days
considered in this work), which would allow the establishment of a better performing
electroactive biofilm at the anode [46,47].
Our study demonstrates for the first time the possibility of harvesting power from
moss with a membrane-less design by using a p-type semiconductor photocatalyst at the
cathode. The simplicity of our system overcomes the limitations of other PMFCs that
use ionic exchange membranes (i.e., membrane accounts the 11% of PMFC
construction costs [48]), thus enhancing the scale-up capability.
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Impedance tests were performed on PMFC-3 and PMFC-4 to estimate the overall
internal resistance in the system [49]. Figure 8C reports the Nyquist plots obtained. A
quantitative analysis of the EIS data was performed through a Randles equivalent circuit
with a Warburg element (inset in Figure 8C). To account for the non-ideal capacitor, a
constant phase element, Q (1/Z=Q(jω)n), was used [50]. In the proposed circuital model,
R2Q2 is accounting for polarisation resistance associated with charge transfer processes
occurring at the cathode/electrolyte interface [44,51–54].
The circuital parameters obtained are summarised in Table S2. The R2 values
obtained suggest a significant decrease of RCT in PMFC-4, compared to PMFC-3, which
implies lower charge transfer resistance when Nafion is used. The R1 values obtained
indicate high resistance due to electrolyte solution, contacts and/or wires [50,52,55].
The Warburg impedance in the equivalent circuit (inset in Figure 8C) is associated
to diffusion effects [52]. Nonetheless, these are overcome by the positive contribution
of the Nafion over-layer, in terms of reduction of RΩ and RCT values. In conclusion,
these results suggest that Nafion plays an important role in reducing the internal
resistance of the system.
Conclusions
We report the first membrane-less light-driven PMFC and demonstrates energy
harvesting from moss. Cathodes functionalised with CuO-Cu2O p-type semiconductors
were implemented, with a Nafion coating to prevent the photocatalyst leaching. Under
irradiation, the photogenerated electrons react with electron acceptors at the cathode/soil
interface. Photogenerated holes at the CuxO valence band serve as acceptors for the
bioelectrons transferred from the anode. Over the six days tested, a 12 times higher
current output was observed with the CuxO cathode, compared to a carbon felt cathode.
The protective coating caused a further 14% increase in the current output.
Although the long-term stability must be addressed in follow-up research, these
results highlight a promising route to enhance the PMFC performance without
compromising its simplicity or complicate its manufacture.
Acknowledgements
The authors thank EPSRC for funding (EP/N005961/1). Emma Freeman thanks the EPSRC-funded Bath/ Bristol/Cardiff Catalysis Centre for Doctoral Training (E.F., EP/L016443/1) for funding her PhD scholarship. Experimental data is available via the University of Bath Research Data Archive.
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Appendix A. Supporting information
Supplementary data associated with this article can be found, in the online version, at
(web link).
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4 REFERENCES
[1] R. Regmi, R. Nitisoravut, J. Ketchaimongkol, A decade of plant-assisted
microbial fuel cells: looking back and moving forward, Biofuels. 7269 (2018) 1–
8. doi:10.1080/17597269.2018.1432272.
[2] P. Bombelli, R.J. Dennis, F. Felder, M.B. Cooper, D. Madras Rajaraman Iyer, J.
Royles, S.T.L. Harrison, A.G. Smith, C.J. Harrison, C.J. Howe, Electrical output
of bryophyte microbial fuel cell systems is sufficient to power a radio or an
environmental sensor, R. Soc. Open Sci. 3 (2016) 160249.
doi:10.1098/rsos.160249.
[3] J.F.H.S. and C.J.N.B. David P. B. T. B. Strik, H. V.M. Hamelers (Bert), Green
electricity production with living plants and bacteria in a fuel cell, Int. J.
ENERGY Res. 32 (2008) 870–876. doi:10.1002/er.1397.
[4] M. Helder, W.-S. Chen, E. Van der Harts, D. Dtrik, J. Hubertus,
HamelersPotting, Electricity production with living plants on a green roof:
environmental performance of the plant-microbial fuel cell, Biofuels, Bioprod.
Biorefining. 6 (2012) 246–256. doi:10.1002/bbb.
[5] A. Schievano, A. Colombo, M. Grattieri, S.P. Trasatti, A. Liberale, P. Tremolada,
C. Pino, P. Cristiani, Floating microbial fuel cells as energy harvesters for signal
transmission from natural water bodies, J. Power Sources. 340 (2017) 80–88.
doi:10.1016/j.jpowsour.2016.11.037.
[6] K. Wetser, J. Liu, C. Buisman, D. Strik, Plant microbial fuel cell applied in
wetlands: Spatial, temporal and potential electricity generation of Spartina
anglica salt marshes and Phragmites australis peat soils, Biomass and Bioenergy.
83 (2015) 543–550. doi:10.1016/j.biombioe.2015.11.006.
[7] S.Y. Sawant, T.H. Han, M.H. Cho, Metal-free carbon-based materials: Promising
electrocatalysts for oxygen reduction reaction in microbial fuel cells, Int. J. Mol.
Sci. 18 (2017). doi:10.3390/ijms18010025.
[8] G. Girishkumar, K. Vinodgopal, P. V. Kamat, Carbon Nanostructures in Portable
Fuel Cells: Single-Walled Carbon Nanotube Electrodes for Methanol Oxidation
and Oxygen Reduction, J. Phys. Chem. B. 108 (2004) 19960–19966.
doi:10.1021/jp046872v.
[9] M. Zhang, Y. Yan, K. Gong, L. Mao, Z. Guo, Y. Chen, Electrostatic layer-by-
layer assembled carbon nanotube multilayer film and its electrocatalytic activity
20
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
for O2 reduction, Langmuir. 20 (2004) 8781–8785. doi:10.1021/la0489231.
[10] T.H. Han, N. Parveen, S.A. Ansari, J.H. Shim, A.T.N. Nguyen, M.H. Cho,
Electrochemically synthesized sulfur-doped graphene as a superior metal-free
cathodic catalyst for oxygen reduction reaction in microbial fuel cells, RSC Adv.
6 (2016) 103446–103454. doi:10.1039/c6ra14114e.
[11] G. Yue, K. Meng, Q. Liu, One-Step Synthesis of N-Doped Carbon and Its
Application as a Cost-Efficient Catalyst for the Oxygen Reduction Reaction in
Microbial Fuel Cells, Chempluschem. 80 (2015) 1133–1138.
doi:10.1002/cplu.201500057.
[12] H. Hou, L. Li, P. de Figueiredo, A. Han, Air-cathode microbial fuel cell array: A
device for identifying and characterizing electrochemically active microbes,
Biosens. Bioelectron. 26 (2011) 2680–2684. doi:10.1016/j.bios.2010.06.037.
[13] S. Cheng, H. Liu, B.E. Logan, Power densities using different cathode catalysts
(Pt and CoTMPP) and polymer binders (Nafion and PTFE) in single chamber
microbial fuel cells, Environ. Sci. Technol. 40 (2006) 364–369.
doi:10.1021/es0512071.
[14] S. You, X. Gong, W. Wang, D. Qi, X. Wang, X. Chen, N. Ren, Enhanced
Cathodic Oxygen Reduction and Power Production of Microbial Fuel Cell Based
on Noble-Metal-Free Electrocatalyst Derived from Metal-Organic Frameworks,
Adv. Energy Mater. 6 (2016) 1–9. doi:10.1002/aenm.201501497.
[15] S. Wang, X. Yang, Y. Zhu, Y. Su, C. Li, Solar-assisted dual chamber microbial
fuel cell with a CuInS2 photocathode, RSC Adv. 4 (2014) 23790–23796.
doi:10.1039/C4RA02488E.
[16] Y. Du, Y. Feng, Y. Qu, J. Liu, N. Ren, H. Liu, Electricity generation and
pollutant degradation using a novel biocathode coupled photoelectrochemical
cell, Environ. Sci. Technol. 48 (2014) 7634–7641. doi:10.1021/es5011994.
[17] C. Goswami, K. Kashyap Hazarika, P. Bharali, Transition metal oxide
nanocatalysts for oxygen reduction reaction, Mater. Sci. Energy Technol. 1
(2018) 117–128. doi:10.1016/j.mset.2018.06.005.
[18] A. Lu, Y. Li, S. Jin, H. Ding, C. Zeng, X. Wang, C. Wang, Microbial Fuel Cell
Equipped with a Photocatalytic Rutile-Coated Cathode, Energy & Fuels. (2009)
200276. doi:10.1021/ef200276y.
[19] N. Touach, V.M. Ortiz-Martínez, M.J. Salar-García, A. Benzaouak, F.
Hernández-Fernández, A. P. de Ríos, M. El Mahi, E.M. Lotfi, On the use of
21
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
ferroelectric material LiNbO3 as novel photocatalyst in wastewater-fed microbial
fuel cells, Particuology. 34 (2017) 147–155. doi:10.1016/j.partic.2017.02.006.
[20] Z. Sun, R. Cao, M. Huang, D. Chen, W. Zheng, L. Lin, Effect of light irradiation
on the photoelectricity performance of microbial fuel cell with a copper oxide
nanowire photocathode, J. Photochem. Photobiol. A Chem. 300 (2015).
doi:10.1016/j.jphotochem.2014.12.003.
[21] J. Bilskie, Soil Water Status: Content and potential: Campbell Scientific, Inc.
App. Note 2S-1. 1784 (2001) 84321.
[22] Y. Feng, Q. Yang, X. Wang, B.E. Logan, Treatment of carbon fiber brush anodes
for improving power generation in air-cathode microbial fuel cells, J. Power
Sources. 195 (2010) 1841–1844. doi:10.1016/j.jpowsour.2009.10.030.
[23] J. Chouler, Á. Cruz-Izquierdo, S. Rengaraj, J.L. Scott, M. Di Lorenzo, A screen-
printed paper microbial fuel cell biosensor for detection of toxic compounds in
water, Biosens. Bioelectron. 102 (2018) 49–56. doi:10.1016/j.bios.2017.11.018.
[24] R.C. Mercado, F. Moussy, In vitro and in vivo mineralization of Nafion
membrane used for implantable glucose sensors, Biosens. Bioelectron. 13 (1998)
133–145. doi:10.1016/S0956-5663(97)00112-7.
[25] L. Hu, Y. Huang, F. Zhang, Q. Chen, CuO/Cu2O composite hollow polyhedrons
fabricated from metal–organic framework templates for lithium-ion battery
anodes with a long cycling life, Nanoscale. 5 (2013) 4186.
doi:10.1039/c3nr00623a.
[26] Y. Yang, D. Xu, Q. Wu, P. Diao, Cu2O/CuO bilayered composite as a high-
efficiency photocathode for photoelectrochemical hydrogen evolution reaction,
Sci. Rep. 6 (2016) 1–13. doi:10.1038/srep35158.
[27] V. Arun, K.R. Sankaran, Nafion coated TiO2 and CuO doped TiO2 modified
glassy carbon and platinum electrodes: Preparation, characterization and
application of enhancement of electrochemical sensitivity for azines, J.
Electroanal. Chem. 769 (2016) 35–41. doi:10.1016/j.jelechem.2016.03.014.
[28] Y. Fu, Z. Poursharifi, M. Ashuri, N. Hashemi, R. Montazami, Development of
Polymeric Porous Membrane for Mediator-Less Microbial Fuel Cells: an
Electrochemical Study, Web.Me.Iastate.Edu. (2013) 1–5.
http://www.web.me.iastate.edu/montazami/publications/conferences/Developmen
t of Polymeric Porous Membrane for Mediatorless Microbial Fuel Cells An
Electrochemical Study.pdf.
22
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
[29] Z. Ghassemi, G. Slaughter, Biological fuel cells and membranes, Membranes
(Basel). 7 (2017). doi:10.3390/membranes7010003.
[30] X. Li, X. Wang, Q. Zhao, Y. Zhang, Q. Zhou, In Situ Representation of
Soil/Sediment Conductivity Using Electrochemical Impedance Spectroscopy,
Sensors. 16 (2016) 625. doi:10.3390/s16050625.
[31] P. Taylor, H. Beyenal, Z. Lewandowski, G. Harkin, Biofouling : The Journal of
Bioadhesion and Biofilm Quantifying Biofilm Structure : Facts and Fiction
Quantifying Biofilm Structure : Facts and Fiction, (2013) 37–41.
doi:10.1080/0892701042000191628.
[32] S. Venkata Mohan, S. Veer Raghavulu, P.N. Sarma, Influence of anodic biofilm
growth on bioelectricity production in single chambered mediatorless microbial
fuel cell using mixed anaerobic consortia, Biosens. Bioelectron. 24 (2008) 41–47.
doi:10.1016/j.bios.2008.03.010.
[33] H. Liu, T.J. Hu, G.M. Zeng, X.Z. Yuan, J.J. Wu, Y. Shen, L. Yin, Electricity
generation using p-nitrophenol as substrate in microbial fuel cell, Int. Biodeterior.
Biodegrad. 76 (2013) 108–111. doi:10.1016/j.ibiod.2012.06.015.
[34] Q.Y. Chen, J.S. Liu, Y. Liu, Y.H. Wang, Hydrogen production on TiO2 nanorod
arrays cathode coupling with bio-anode with additional electricity generation, J.
Power Sources. 238 (2013) 345–349. doi:10.1016/j.jpowsour.2013.04.066.
[35] L. Zhang, Y.-C. Zhu, Y.Y. Liang, W.-W. Zhao, J.-J. Xu, H.-Y. Chen,
Semiconducting CuO Nanotubes: Synthesis, Characterization, and Bifunctional
Photocathodic Enzymatic Bioanalysis, Anal. Chem. (2018)
acs.analchem.8b00742. doi:10.1021/acs.analchem.8b00742.
[36] A. Lu, Y. Li, S. Jin, H. Ding, C. Zeng, X. Wang, C. Wang, Microbial fuel cell
equipped with a photocatalytic rutile-coated cathode, Energy and Fuels. 24
(2010) 1184–1190. doi:10.1021/ef901053j.
[37] S. Liu, H. Song, X. Li, F. Yang, Power generation enhancement by utilizing plant
photosynthate in microbial fuel cell coupled constructed wetland system, Int. J.
Photoenergy. 2013 (2013). doi:10.1155/2013/172010.
[38] D.K. Paul, A. Fraser, K. Karan, Towards the understanding of proton conduction
mechanism in PEMFC catalyst layer: Conductivity of adsorbed Nafion films,
Electrochem. Commun. 13 (2011) 774–777. doi:10.1016/j.elecom.2011.04.022.
[39] S.C. DeCaluwe, A.M. Baker, P. Bhargava, J.E. Fischer, J.A. Dura, Structure-
property relationships at Nafion thin-film interfaces: Thickness effects on
23
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
hydration and anisotropic ion transport, Nano Energy. 46 (2018) 91–100.
doi:10.1016/j.nanoen.2018.01.008.
[40] M. Rahimnejad, G. Bakeri, G. Najafpour, M. Ghasemi, S. Oh, A review on the
effect of proton exchange membranes in microbial fuel cells, Biofuel Res. J. 1
(2014) 7–15. doi:10.18331/BRJ2015.1.1.4.
[41] M. Hans, A. Erbe, S. Mathews, Y. Chen, M. Solioz, F. Mücklich, Role of copper
oxides in contact killing of bacteria, Langmuir. 29 (2013) 16160–16166.
doi:10.1021/la404091z.
[42] O. Bondarenko, K. Juganson, A. Ivask, K. Kasemets, M. Mortimer, A. Kahru,
Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant
test organisms and mammalian cells in vitro: A critical review, Arch. Toxicol. 87
(2013) 1181–1200. doi:10.1007/s00204-013-1079-4.
[43] X.-W. Liu, W.-W. Li, H.-Q. Yu, Cathodic catalysts in bioelectrochemical
systems for energy recovery from wastewater, Chem. Soc. Rev. 43 (2014) 7718–
7745. doi:10.1039/C3CS60130G.
[44] N.S. Ramaraja P Ramasamy, Electrochemical Impedance Spectroscopy for
Microbial Fuel Cell Characterization, J. Microb. Biochem. Technol. (2013).
doi:10.4172/1948-5948.S6-004.
[45] N. Kaku, N. Yonezawa, Y. Kodama, K. Watanabe, Plant/microbe cooperation for
electricity generation in a rice paddy field, Appl. Microbiol. Biotechnol. 79
(2008) 43–49. doi:10.1007/s00253-008-1410-9.
[46] Z. Ren, R.P. Ramasamy, S.R. Cloud-Owen, H. Yan, M.M. Mench, J.M. Regan,
Time-course correlation of biofilm properties and electrochemical performance in
single-chamber microbial fuel cells, Bioresour. Technol. 102 (2011) 416–421.
doi:10.1016/j.biortech.2010.06.003.
[47] B. Hou, Y.-Y. Hu, J. Sun, Y.-Q. Cao, Effect of Anodic Biofilm Growth on the
Performance of the Microbial Fuel Cell (MFC), 2010 4th Int. Conf. Bioinforma.
Biomed. Eng. (2010) 1–4. doi:10.1109/ICBBE.2010.5514877.
[48] R. Nitisoravut, R. Regmi, Plant microbial fuel cells: A promising biosystems
engineering, Renew. Sustain. Energy Rev. 76 (2017) 81–89.
doi:10.1016/j.rser.2017.03.064.
[49] R.P. Ramasamy, Z. Ren, M.M. Mench, J.M. Regan, Impact of initial biofilm
growth on the anode impedance of microbial fuel cells, Biotechnol. Bioeng. 101
(2008) 101–108. doi:10.1002/bit.21878.
24
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
[50] S. Palmas, P.A. Castresana, L. Mais, A. Vacca, M. Mascia, P.C. Ricci, TiO2 –
WO3 nanostructured systems for photoelectrochemical applications, RSC Adv. 6
(2016) 101671–101682. doi:10.1039/C6RA18649A.
[51] Z. He, N. Wagner, S.D. Minteer, L.T. Angenent, An upflow microbial fuel cell
with an interior cathode: Assessment of the internal resistance by impedance
spectroscopy, Environ. Sci. Technol. 40 (2006) 5212–5217.
doi:10.1021/es060394f.
[52] S.-M. Park, J.-S. Yoo, Electrochemical Impedance Spectroscopy for Better
Electrochemical Measurements, Anal. Chem. 75 (2003) 455 A-461 A.
doi:10.1021/ac0313973.
[53] P. Electrochemistry, C. Elements, C. Equivalent, C. Models, Basics of
Electrochemical Impedance Spectroscopy, Appl. Note AC. 286 (2010) R491-7.
doi:10.1152/ajpregu.00432.2003.
[54] P. Liang, X. Huang, M.Z. Fan, X.X. Cao, C. Wang, Composition and distribution
of internal resistance in three types of microbial fuel cells, Appl. Microbiol.
Biotechnol. 77 (2007) 551–558. doi:10.1007/s00253-007-1193-4.
[55] G. Lepage, F.O. Albernaz, G. Perrier, G. Merlin, Characterization of a microbial
fuel cell with reticulated carbon foam electrodes, Bioresour. Technol. 124 (2012)
199–207. doi:10.1016/j.biortech.2012.07.067.
25
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
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18
19
20
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